Colorado mountains

Organic matter contribution and decomposition by ectomycorrhizal fungi in response to chronic nitrogen deposition in a temperate mixed-hardwood forest

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Jesse Sadowsky
Linda T.A. van Diepen
Serita D. Frey

Ectomycorrhizal (ECM) fungi comprise a large proportion of total soil microbial biomass, contribute belowground inputs as mycelia that may equal or surpass those of roots, and secrete enzymes that catalyze organic matter decomposition. ECM fungi therefore play a major role in biogeochemical processes in forest ecosystems. Surprising, though, functional responses ECM fungi to anthropogenic stressors such as N deposition are not well documented. In the 25th year of the Chronic Nitrogen Addition Study in a mixed-hardwood stand at Harvard Forest, Petersham, MA, USA, we are evaluating responses of extraradical ECM mycelial growth and ECM fungal enzyme production to ambient, low (5 g m-2 yr-1), and high (15 g m-2 yr-1) rates of N deposition. Extraradical mycelium is collected in root-delimited in-growth bags buried in soil for one growing season. Activity of hydrolytic and oxidative enzymes catalyzing decomposition of organic C, N, and P polymers in soil is assessed on the outer fungal mantle of ECM roots collected from organic and mineral soil horizons on six dates over 12 months. Enzyme activity in bulk soil is also assessed to compare responses of ECM fungi and total soil microbial communities to long-term N enrichment. In 2011, extraradical ECM mycelial growth was 15% less under both low and high N deposition rates, which agrees with reduced total (ectomycorrhizal and saprotrophic) soil fungal biomass under N deposition observed previously at this site. Over three sampling dates between November 2011 and July 2012, N enrichment consistently altered enzyme production by ECM fungi, and responses of ECM fungi to N enrichment occurred either in line with or counter to total soil microbial communities. Under low and high N deposition, ECM fungal carbohydrolase (cellobiohydrolase, B-glucosidase, and chitinase) activity increased and aminopeptidase activity declined in a stepwise fashion in the organic soil horizon, with similar but slightly attenuated responses in the underlying mineral soil. N enrichment effects on ECM fungal carbohydrolase and aminopeptidase production correlated well with those in bulk soil, suggesting N availability exerts a similar control on stoichiometry of enzymatic C and N acquisition from soil organic matter by ECM fungi as that of free-living decomposers. By contrast, at peak values in July, oxidative activity of ECM fungi was highest in soil receiving the highest N deposition rate and having the lowest oxidative potential, implying that ECM fungi contribute more strongly to oxidative soil organic matter transformations under long-term N enrichment even as total oxidative activity in soil declines. This may constitute a physiological adaptation of ECM fungal communities to accrual of aromatic-rich organic matter that has occurred in N-enriched soils at this site. Unexpectedly, phosphatase activity of ECM fungi has so far been unresponsive to chronic N deposition. Based on these observations, we hypothesize that, following exposure to long-term N enrichment, ECM fungi in Harvard Forest have transitioned from latent to active decomposers of soil C. We are currently identifying fungi on ECM root tips, preserved in storage following enzyme assays, to assess whether ECM fungal species occupy unique functional niches in soil organic matter decomposition, and to determine if N deposition-mediated changes in community-scale ECM fungal enzyme production correspond to an altered makeup of ECM fungal communities. Further efforts to resolve whether extracellular carbohydrolase and oxidase production by ECM fungi reflects their proportion of soil organic matter- vs. plant symbiont-derived C supply, and whether long-term N enrichment alters the balance of ECM vs. saprotrophic fungal decomposition pathways in soil may allow for a more mechanistic, robust prediction of soil C dynamics in forests subjected to anthropogenic N deposition.

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Background Photo by: Nicole Hansen - Jornada (JRN) LTER